Current evidence suggests evolution is guided by environment as much as genes, but most people still think genes are in the driver's seat.

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In a terrific and controversial essay in Aeon magazine yesterday, science journalist David Dobbs has done a careful job unpacking how Dawkins' brilliant book, The Selfish Gene, has outlived its usefulness. Published in 1976, The Selfish Gene was the most elegant summary of cutting-edge genetic theory at the time. More importantly, it was written for a popular audience, which ate the book up and made it a bestseller. Perhaps the most catchy part of the book was its title, a slightly hyperbolic twist on the book's main thesis: that evolution is driven by competition between genes, as well as between organisms and species.

Like I said, at the time it was published, this was a notion that few people outside the scientific community understood. And Dawkins helped millions of people understand this crucial idea, which remains true. It's just not the full story, as Dobbs reveals in interview after interview with scientists who currently study genes and evolution.

"We have a more complicated understanding of football than we do genetics and evolution. Nobody thinks just the quarterback wins the game," says biologist Gregory Wray, comparing the gene to the quarterback. "We're stuck in an outmoded way of thinking that should have fallen long ago." Evolutionary biologist Mary Jane West-Eberhard puts it more simply: "The gene does not lead. It follows." This is the same argument that MIT's Evelyn Fox Keller made 14 years ago in her book The Century of the Gene.

To be clear, biologists like West-Eberhard and others are not saying genes and their selfishness aren't important. But they are merely one part of a much larger and more complicated mechanism, which involves inputs from the environment which affect how genes express themselves.

So what replaces the selfish gene in this new model of evolutionary change? From his interviews with scientists, Dobbs believes a good contender would be the idea of "genetic accommodation," which explains how the gene fits into this larger machinery (or, to continue Wray's metaphor, into the football game). It's worth quoting at length from Dobbs here:

Genetic accommodation involves a three-step process.

First, an organism (or a bunch of organisms, a population) changes its functional form — its phenotype — by making broad changes in gene expression. Second, a gene emerges that happens to help lock in that change in phenotype. Third, the gene spreads through the population.

For example, suppose you're a predator. You live with others of your ilk in dense forest. Your kind hunts by stealth: you hide among trees, then jump out and snag your meat. You needn't be fast, just quick and sneaky.

Then a big event — maybe a forest fire, or a plague that kills all your normal prey — forces you into a new environment. This new place is more open, which nixes your jump-and-grab tactic, but it contains plump, juicy animals, the slowest of which you can outrun if you sprint hard. You start running down these critters. As you do, certain genes ramp up expression to build more muscle and fire the muscles more quickly. You get faster. You're becoming a different animal. You mate with another fast hunter, and your kids, hunting with you from early on, soon run faster than you ever did. Via gene expression, they develop leaner torsos and more muscular, powerful legs. By the time your grandchildren show up, they seem almost like different animals: stronger legs, leaner torsos, and they run way faster than you ever did. And all this has happened without taking on any new genes.

Then a mutation occurs in one grandkid. This mutation happens to create stronger, faster muscle fibres. This grandchild of yours can naturally and easily run faster than her fastest siblings and cousins. She flies. Her children inherit the gene, and because their speed wows their mating prospects, they mate early and often, and bear lots of kids. Through the generations, this sprinter's gene thus spreads through the population.

Now the thing is complete. Your descendants have a new gene that helps secure the adaptive trait you originally developed through gene expression alone. But the new gene didn't create the new trait. It just made it easier to keep a trait that a change in the environment made valuable. The gene didn't drive the train; it merely hopped aboard. Had the gene showed up earlier (either through mutation or mating with an outsider), back when you lived in the forest and speed didn't mean anything, it would have given no advantage. Instead of being selected for and spreading, the gene would have disappeared or remained in just a few animals. But because the gene was now of value, the population took it in, accommodated it, and spread it wide.

The problem is that this account is complicated — there is no easy causal relationship between gene and phenotype. Dawkins' model has retained its grip on the public imagination because it's simple enough to go viral as an idea. Which was great back in the 1970s, when our understanding of genes was itself relatively simple. But today, in the wake of rapid genetic sequencing and advances in population genetics, most scientists include genes as one part of a much bigger picture.

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Except, apparently, Dawkins himself. When Dobbs asked Dawkins what he thought of the accommodation model, Dawkins claimed that it didn't unseat the gene as the main driver of evolutionary change because the gene cemented the phenotypic changes brought about by environment. And when Dobbs published his article yesterday, Dawkins claimed on Twitter that he "could have written" Dobbs' article because it contained nothing that he hadn't already covered in his 1976 book. Even though his book was written before any genomes had been sequenced, and before the explosion of discoveries in epigenetics, which is the study of how environment shapes gene expression. Later, Dawkins simply advised his followers:

Needless to say, this is an excellent way to refuse to engage. Instead of responding to the questions that people are raising, simply claim that everything resides in the good book — if you'll only read it correctly.

The irony is that nobody is actually claiming that Dawkins is wrong. They're just saying that "the selfish gene" doesn't give us a complete picture of how evolution works. In the 38 years since its publication, evolutionary biologists have worked out that the whole thing is a lot more complicated than "selfish genes." As geneticist Michael Eisen puts it to Dobbs:

Evolution is not even that simple. Anyone who's worked on systems sees that natural selection takes advantage of the most bizarre aspects of biology. When something has so many parts, evolution will act on all of them. It's not that genes don't sometimes drive evolutionary change. It's that this mutational model — a gene changes, therefore the organism changes — is just one way to get the job done. Other ways may actually do more.

And this doesn't even get into the ways that organism evolution may be shaped by microbiomes, or the vast ecosystems of microbes that live in and on our bodies. The problem is that we don't yet have a meme that's as catchy as "the selfish gene" to explain the "other ways" model that Eisen and his contemporaries are working with. And this is ultimately what Dobbs' essay is about.

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We need a better way of explaining the genetics of evolution to people who don't work in labs and read scientific journals. The Selfish Gene was a pop science masterpiece of a bygone age. Now we need to build a new public understanding of evolution that puts the selfish gene in its place, as a player alongside many others in the ongoing drama of mutation and evolutionary change.

What snappy phrase will sum up genetic accommodation and epigenetics? Maybe the answer is that we don't need one, but many. That would be in keeping with what we've learned about evolution itself. There is no one unit of information that leads our transformation as a species. Instead there are a lot of factors affecting change, sometimes working together — and sometimes at odds.